CCR5 promoter haplotypes differentially influence CCR5 expression on natural killer and T cell subsets in ethnically divergent HIV-1 uninfected South African populations

Immunogenetics

Volumn 64, Issue 11, 2012, Pages 795-806

  Picton, Anabela C P ^a,b   Paximadis, Maria ^a,b   Tiemessen, Caroline T ^a,b  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

CCR5 expression; CCR5 haplotypes; HIV 1; Natural killer cells; South African populations; T cells

Indexed keywords

CHEMOKINE RECEPTOR CCR5; GENOMIC DNA;

ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; COHORT ANALYSIS; DISEASE PREDISPOSITION; ETHNIC GROUP; FLOW CYTOMETRY; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NATURAL KILLER CELL; NORMAL HUMAN; POPULATION GENETICS; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SOUTH AFRICA; T LYMPHOCYTE SUBPOPULATION;

ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; CROSS-SECTIONAL STUDIES; DISEASE PROGRESSION; DNA, VIRAL; EUROPEAN CONTINENTAL ANCESTRY GROUP; FLOW CYTOMETRY; HAPLOTYPES; HIV INFECTIONS; HIV-1; HUMANS; KILLER CELLS, NATURAL; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RECEPTORS, CCR5; T-LYMPHOCYTE SUBSETS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84867876693     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-012-0642-0     Document Type: Article

References (65)

1. Alter G, Altfeld M (2009) NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 265:29-42
2. An P, Martin MP, Nelson GW, Carrington M, Smith MW, Gong K, Vlahov D, O'Brien SJ, Winkler CA (2000) Influence of CCR5 promoter haplotypes on AIDS progression in African-Americans. AIDS 14:2117-2122
3. Ansari-Lari MA, Liu XM, Metzker ML, Rut AR, Gibbs RA (1997) The extent of genetic variation in the CCR5 gene. Nat Genet 16:221-222
4. Begaud E, Chartier L, Marechal V, Ipero J, Leal J, Versmisse P, Breton G, Fontanet A, Capoulade-Metay C, Fleury H, Barre-Sinoussi F, Scott-Algara D, Pancino G (2006) Reduced CD4 T cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3:35
5. Carrington M, Kissner T, Gerrard B, Ivanov S, O'Brien SJ, Dean M (1997) Novel alleles of the chemokine-receptor gene CCR5. Am J Hum Genet 61:1261-1267
6. de Roda Husman AM, Blaak H, Brouwer M, Schuitemaker H (1999) CC chemokine receptor 5 cell-surface expression in relation to CC chemokine receptor 5 genotype and the clinical course of HIV-1 infection. J Immunol 163:4597-4603
7. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, Allikmets R, Goedert JJ, Buchbinder SP, Vittinghoff E, Gomperts E, Donfield S, Vlahov D, Kaslow R, Saah A, Rinaldo C, Detels R, O'Brien SJ (1996) Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia growth and development study, multicenter AIDS cohort study, multicenter hemophilia cohort study, San Francisco City Cohort, ALIVE Study. Science 273:1856-1862
8. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666
9. Desmetz C, Lin YL, Mettling C, Portales P, Rabesandratana H, Clot J, Corbeau P (2006) The strength of the chemotactic response to a CCR5 binding chemokine is determined by the level of cell surface CCR5 density. Immunology 119:551-561
10. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673
11. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ (2006) Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 20:73-83
12. Galvani AP, Novembre J (2005) The evolutionary history of the CCR5-Delta32 HIV-resistance mutation. Microbes Infect 7:302-309
13. Gonzalez E, Bamshad M, Sato N, Mummidi S, Dhanda R, Catano G, Cabrera S, McBride M, Cao XH, Merrill G, O'Connell P, Bowden DW, Freedman BI, Anderson SA, Walter EA, Evans JS, Stephan KT, Clark RA, Tyagi S, Ahuja SS, Dolan MJ, Ahuja SK (1999) Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes. Proc Natl Acad Sci U S A 96:12004-12009
14. Gonzalez E, Dhanda R, Bamshad M, Mummidi S, Geevarghese R, Catano G, Anderson SA, Walter EA, Stephan KT, Hammer MF, Mangano A, Sen L, Clark RA, Ahuja SS, Dolan MJ, Ahuja SK (2001) Global survey of genetic variation in CCR5, RANTES, and MIP-1alpha: impact on the epidemiology of the HIV-1 pandemic. Proc Natl Acad Sci U S A 98:5199-5204
15. Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, Catano G, Nibbs RJ, Freedman BI, Quinones MP, Bamshad MJ, Murthy KK, Rovin BH, Bradley W, Clark RA, Anderson SA, O'Connell RJ, Agan BK, Ahuja SS, Bologna R, Sen L, Dolan MJ, Ahuja SK (2005) The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307:1434-1440
16. Howard OM, Shirakawa AK, Turpin JA, Maynard A, Tobin GJ, Carrington M, Oppenheim JJ, Dean M (1999) Naturally occurring CCR5 extracellular and transmembrane domain variants affect HIV-1 Co-receptor and ligand binding function. J Biol Chem 274:16228-16234
17. John GC, Bird T, Overbaugh J, Nduati R, Mbori-Ngacha D, Rostron T, Dong T, Kostrikis L, Richardson B, Rowland-Jones SL (2001) CCR5 promoter polymorphisms in a Kenyan perinatal human immunodeficiency virus type 1 cohort: association with increased 2-year maternal mortality. J Infect Dis 184:89-92
18. Kalinkovich A, Borkow G, Weisman Z, Tsimanis A, Stein M, Bentwich Z (2001) Increased CCR5 and CXCR4 expression in Ethiopians living in Israel: environmental and constitutive factors. Clin Immunol 100:107-117
19. Ketas TJ, Kuhmann SE, Palmer A, Zurita J, He W, Ahuja SK, Klasse PJ, Moore JP (2007) Cell surface expression of CCR5 and other host factors influence the inhibition of HIV-1 infection of human lymphocytes by CCR5 ligands. Virology 364:281-290
20. Khan IA, Thomas SY, Moretto MM, Lee FS, Islam SA, Combe C, Schwartzman JD, Luster AD (2006) CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog 2:e49
21. Kostrikis LG, Huang Y, Moore JP, Wolinsky SM, Zhang L, Guo Y, Deutsch L, Phair J, Neumann AU, Ho DD (1998) A chemokine receptor CCR2 allele delays HIV-1 disease progression and is associated with a CCR5 promoter mutation. Nat Med 4:350-353
22. Kostrikis LG, Neumann AU, Thomson B, Korber BT, McHardy P, Karanicolas R, Deutsch L, Huang Y, Lew JF, McIntosh K, Pollack H, Borkowsky W, Spiegel HM, Palumbo P, Oleske J, Bardeguez A, Luzuriaga K, Sullivan J, Wolinsky SM, Koup RA, Ho DD, Moore JP (1999) A polymorphism in the regulatory region of the CC-chemokine receptor 5 gene influences perinatal transmission of human immunodeficiency virus type 1 to African-American infants. J Virol 73:10264-10271
23. Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW (1999) Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci U S A 96:5215-5220
24. Li M, Song R, Masciotra S, Soriano V, Spira TJ, Lal RB, Yang C (2005) Association of CCR5 human haplogroup E with rapid HIV type 1 disease progression. AIDS Res Hum Retroviruses 21:111-115
25. Lin YL, Mettling C, Portales P, Rouzier R, Clot J, Reynes J, Corbeau P (2008) The chemokine CCL5 regulates the in vivo cell surface expression of its receptor, CCR5. AIDS 22:430-432
26. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, MacDonald ME, Stuhlmann H, Koup RA, Landau NR (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377
27. Liu Y, Liu FL, He Y, Li L, Li S, Zheng YT, Wang H, Gong X (2012) The genetic variation of CCR5, CXCR4 and SDF-1 in three Chinese ethnic populations. Infect Genet Evol 12:1072-1078
28. Magierowska M, Lepage V, Lien TX, Lan NT, Guillotel M, Issafras H, Reynes JM, Fleury HJ, Chi NH, Follezou JY, Debre P, Theodorou I, Barre-Sinoussi F (1999) Novel variant of the CCR5 gene in a Vietnamese population. Microbes Infect 1:123-124
29. Malhotra R, Hu L, Song W, Brill I, Mulenga J, Allen S, Hunter E, Shrestha S, Tang J, Kaslow RA (2011) Association of chemokine receptor gene (CCR2-CCR5) haplotypes with acquisition and control of HIV-1 infection in Zambians. Retrovirology 8:22
30. Mamtani M, Mummidi S, Ramsuran V, Pham MH, Maldonado R, Begum K, Valera MS, Sanchez R, Castiblanco J, Kulkarni H, Ndung'u T, He W, Anaya JM, Ahuja SK (2011) Influence of variations in CCL3L1 and CCR5 on tuberculosis in a northwestern Colombian population. J Infect Dis 203:1590-1594
31. Mangano A, Gonzalez E, Dhanda R, Catano G, Bamshad M, Bock A, Duggirala R, Williams K, Mummidi S, Clark RA, Ahuja SS, Dolan MJ, Bologna R, Sen L, Ahuja SK (2001) Concordance between the CC chemokine receptor 5 genetic determinants that alter risks of transmission and disease progression in children exposed perinatally to human immunodeficiency virus. J Infect Dis 183:1574-1585
32. Martin MP, Dean M, Smith MW, Winkler C, Gerrard B, Michael NL, Lee B, Doms RW, Margolick J, Buchbinder S, Goedert JJ, O'Brien TR, Hilgartner MW, Vlahov D, O'Brien SJ, Carrington M (1998) Genetic acceleration of AIDS progression by a promoter variant of CCR5. Science 282:1907-1911
33. Masquelier C, Servais JY, Rusanganwa E, Roman F, Havuga E, Servais J, Tuyizere S, Omes C, Karasi JC, Coruteille O, Karita E, Allen S, Schmit JC, Arendt V (2007) A novel 24-base pair deletion in the coding region of CCR5 in an African population. AIDS 21:111-113
34. McDermott DH, Zimmerman PA, Guignard F, Kleeberger CA, Leitman SF, Murphy PM (1998) CCR5 promoter polymorphism and HIV-1 disease progression. Multicenter AIDS Cohort Study (MACS). Lancet 352:866-870
35. Meditz AL, Haas MK, Folkvord JM, Melander K, Young R, McCarter M, Mawhinney S, Campbell TB, Lie Y, Coakley E, Levy DN, Connick E (2011) HLA-DR+CD38+ CD4+ T lymphocytes have elevated CCR5 expression and produce the majority of R5-tropic HIV-1 RNA in vivo. J Virol 85:10189-10200
36. Moore JP, Trkola A, Dragic T (1997) Co-receptors for HIV-1 entry. Curr Opin Immunol 9:551-562
37. Moriuchi H, Moriuchi M, Fauci AS (1997) Cloning and analysis of the promoter region of CCR5, a coreceptor for HIV-1 entry. J Immunol 159:5441-5449
38. Mummidi S, Bamshad M, Ahuja SS, Gonzalez E, Feuillet PM, Begum K, Galvis MC, Kostecki V, Valente AJ, Murthy KK, Haro L, Dolan MJ, Allan JS, Ahuja SK (2000) Evolution of human and non-human primate CC chemokine receptor 5 gene and mRNA. Potential roles for haplotype and mRNA diversity, differential haplotype-specific transcriptional activity, and altered transcription factor binding to polymorphic nucleotides in the pathogenesis of HIV-1 and simian immunodeficiency virus. J Biol Chem 275:18946-18961
39. Nguyen L, Li M, Chaowanachan T, Hu DJ, Vanichseni S, Mock PA, van Griensven F, Martin M, Sangkum U, Choopanya K, Tappero JW, Lal RB, Yang C (2004) CCR5 promoter human haplogroups associated with HIV-1 disease progression in Thai injection drug users. AIDS 18:1327-1333
40. Niu T, Qin ZS, Xu X, Liu JS (2002) Bayesian haplotype inference for multiple linked single-nucleotide polymorphisms. Am J Hum Genet 70:157-169
41. Ometto L, Bertorelle R, Mainardi M, Zanchetta M, Tognazzo S, Rampon O, Ruga E, Chieco-Bianchi L, De Rossi A (2001) Polymorphisms in the CCR5 promoter region influence disease progression in perinatally human immunodeficiency virus type 1-infected children. J Infect Dis 183:814-818
42. Ostrowski MA, Justement SJ, Catanzaro A, Hallahan CA, Ehler LA, Mizell SB, Kumar PN, Mican JA, Chun TW, Fauci AS (1998) Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. J Immunol 161:3195-3201
43. Petersen DC, Kotze MJ, Zeier MD, Grimwood A, Pretorius D, Vardas E, van Rensburg EJ, Hayes VM (2001) Novel mutations identified using a comprehensive CCR5-denaturing gradient gel electrophoresis assay. AIDS 15:171-177
44. Picton AC, Paximadis M, Tiemessen CT (2010) Genetic variation within the gene encoding the HIV-1 CCR5 coreceptor in two South African populations. Infect Genet Evol 10:487-494
45. Picton AC, Shalekoff S, Paximadis M, Tiemessen CT (2012) Marked differences in CCR5 expression and activation levels in two South African populations. Immunology 136:397-407
46. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D (1998) Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72:2855-2864
47. Quillent C, Oberlin E, Braun J, Rousset D, Gonzalez-Canali G, Metais P, Montagnier L, Virelizier JL, Arenzana-Seisdedos F, Beretta A (1998) HIV-1-resistance phenotype conferred by combination of two separate inherited mutations of CCR5 gene. Lancet 351:14-18
48. Reynes J, Portales P, Segondy M, Baillat V, Andre P, Reant B, Avinens O, Couderc G, Benkirane M, Clot J, Eliaou JF, Corbeau P (2000) CD4+ T cell surface CCR5 density as a determining factor of virus load in persons infected with human immunodeficiency virus type 1. J Infect Dis 181:927-932
49. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M (1996) Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722-725
50. Scott-Algara D, Truong LX, Versmisse P, David A, Luong TT, Nguyen NV, Theodorou I, Barre-Sinoussi F, Pancino G (2003) Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J Immunol 171:5663-5667
51. Shalekoff S, Tiemessen CT (2003) CCR5 delta32 heterozygosity is associated with an increase in CXCR4 cell surface expression. AIDS Res Hum Retroviruses 19:531-533
52. Shalekoff S, Pendle S, Johnson D, Martin DJ, Tiemessen CT (2001) Distribution of the human immunodeficiency virus coreceptors CXCR4 and CCR5 on leukocytes of persons with human immunodeficiency virus type 1 infection and pulmonary tuberculosis: implications for pathogenesis. J Clin Immunol 21:390-401
53. Shioda T, Nakayama EE, Tanaka Y, Xin X, Liu H, Kawana-Tachikawa A, Kato A, Sakai Y, Nagai Y, Iwamoto A (2001) Naturally occurring deletional mutation in the C-terminal cytoplasmic tail of CCR5 affects surface trafficking of CCR5. J Virol 75:3462-3468
54. Singh KK, Hughes MD, Chen J, Phiri K, Rousseau C, Kuhn L, Coutsoudis A, Jackson JB, Guay LA, Musoke P, Mmiro F, Semba RD, Spector SA (2008) Associations of chemokine receptor polymorphisms With HIV-1 mother-to-child transmission in sub-Saharan Africa: possible modulation of genetic effects by antiretrovirals. J Acquir Immune Defic Syndr 49:259-265
55. Tang J, Shelton B, Makhatadze NJ, Zhang Y, Schaen M, Louie LG, Goedert JJ, Seaberg EC, Margolick JB, Mellors J, Kaslow RA (2002) Distribution of chemokine receptor CCR2 and CCR5 genotypes and their relative contribution to human immunodeficiency virus type 1 (HIV-1) seroconversion, early HIV-1 RNA concentration in plasma, and later disease progression. J Virol 76:662-672
56. Thapa M, Kuziel WA, Carr DJ (2007) Susceptibility of CCR5-deficient mice to genital herpes simplex virus type 2 is linked to NK cell mobilization. J Virol 81:3704-3713
57. Tiemessen CT, Shalekoff S, Meddows-Taylor S, Schramm DB, Papathanasopoulos MA, Gray GE, Sherman GG, Coovadia AH, Kuhn L (2009) Cutting edge: unusual NK cell responses to HIV-1 peptides are associated with protection against maternal-infant transmission of HIV-1. J Immunol 182:5914-5918
58. Tiemessen CT, Shalekoff S, Meddows-Taylor S, Schramm DB, Papathanasopoulos MA, Gray GE, Sherman GG, Coovadia AH, Kuhn L (2010) Natural killer cells that respond to human immunodeficiency virus type 1 (HIV-1) peptides are associated with control of HIV-1 infection. J Infect Dis 202:1444-1453
59. Uitenbroek DG (1997) SISA-Binomial. http://quantitativeskills.com/sisa/ distributions/binomial
60. Weiss ID, Shoham H, Wald O, Wald H, Beider K, Abraham M, Barashi N, Galun E, Nagler A, Peled A (2011) Ccr5 deficiency regulates the proliferation and trafficking of natural killer cells under physiological conditions. Cytokine 54:249-257
61. Weissman D, Dybul M, Daucher MB, Davey RT Jr, Walker RE, Kovacs JA (2000) Interleukin-2 up-regulates expression of the human immunodeficiency virus fusion coreceptor CCR5 by CD4+ lymphocytes in vivo. J Infect Dis 181:933-938
62. Wu L, Paxton WA, Kassam N, Ruffing N, Rottman JB, Sullivan N, Choe H, Sodroski J, Newman W, Koup RA, Mackay CR (1997) CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J Exp Med 185:1681-1691
63. Yang YF, Tomura M, Iwasaki M, Mukai T, Gao P, Ono S, Zou JP, Shearer GM, Fujiwara H, Hamaoka T (2001a) IL-12 as well as IL-2 upregulates CCR5 expression on T cell receptor-triggered human CD4+ and CD8+ T cells. J Clin Immunol 21:116-125
64. Yang YF, Tomura M, Iwasaki M, Ono S, Zou JP, Uno K, Shearer GM, Fujiwara H, Hamaoka T (2001b) IFN-alpha acts on T-cell receptor-triggered human peripheral leukocytes to up-regulate CCR5 expression on CD4+ and CD8+ T cells. J Clin Immunol 21:402-409
65. Zou W, Foussat A, Houhou S, Durand-Gasselin I, Dulioust A, Bouchet L, Galanaud P, Levy Y, Emilie D (1999) Acute upregulation of CCR-5 expression by CD4+ T lymphocytes in HIV-infected patients treated with interleukin-2. ANRS 048 IL-2 Study Group. AIDS 13:455-463